Dynamical allosterism in the mechanism of action of DNA mismatch repair protein MutS

Biophysical Journal

Volumn 101, Issue 7, 2011, Pages 1730-1739

  Pieniazek, Susan N ^a   Hingorani, Manju M ^a   Beveridge, D L ^a  

^a WESLEYAN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; PROTEIN MUTS;

ALLOSTERISM; ARTICLE; CHEMISTRY; ENZYMOLOGY; METABOLISM; MISMATCH REPAIR; MOLECULAR DYNAMICS; PROTEIN TERTIARY STRUCTURE; THERMUS;

ADENOSINE TRIPHOSPHATE; ALLOSTERIC REGULATION; DNA MISMATCH REPAIR; MOLECULAR DYNAMICS SIMULATION; MUTS DNA MISMATCH-BINDING PROTEIN; PROTEIN STRUCTURE, TERTIARY; THERMUS;

EUKARYOTA; PROKARYOTA; THERMUS AQUATICUS;

EID: 80053350446     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.08.039     Document Type: Article

References (70)

1. T.A. Kunkel, and D.A. Erie DNA mismatch repair Annu. Rev. Biochem. 74 2005 681 710 (Pubitemid 40995521)
2. E. Renkonen, and Y. Zhang P. Peltomaki Altered expression of MLH1, MSH2, and MSH6 in predisposition to hereditary nonpolyposis colorectal cancer J. Clin. Oncol. 21 2003 3629 3637 (Pubitemid 46594056)
3. R.D. Kolodner Mismatch repair: mechanisms and relationship to cancer susceptibility Trends Biochem. Sci. 20 1995 397 401
4. J. Jiricny MutLalpha: at the cutting edge of mismatch repair Cell 126 2006 239 241 (Pubitemid 44092971)
5. P. Hsieh, and K. Yamane DNA mismatch repair: molecular mechanism, cancer, and ageing Mech. Ageing Dev. 129 2008 391 407
6. R.R. Iyer, and A. Pluciennik P. Modrich MutLα and proliferating cell nuclear antigen share binding sites on MutSβ J. Biol. Chem. 285 2010 11730 11739
7. C. Kunz, Y. Saito, and P. Schär DNA repair in mammalian cells: mismatched repair: variations on a theme Cell. Mol. Life Sci. 66 2009 1021 1038
8. R.D. Kolodner, M.L. Mendillo, and C.D. Putnam Coupling distant sites in DNA during DNA mismatch repair Proc. Natl. Acad. Sci. USA 104 2007 12953 12954 (Pubitemid 351737574)
9. M.L. Mendillo, D.J. Mazur, and R.D. Kolodner Analysis of the interaction between the Saccharomyces cerevisiae MSH2-MSH6 and MLH1-PMS1 complexes with DNA using a reversible DNA end-blocking system J. Biol. Chem. 280 2005 22245 22257 (Pubitemid 40827881)
10. S. Acharya, and P.L. Foster R. Fishel The coordinated functions of the E. coli MutS and MutL proteins in mismatch repair Mol. Cell 12 2003 233 246 (Pubitemid 36945047)
11. T. Selmane, and M.J. Schofield P. Hsieh Formation of a DNA mismatch repair complex mediated by ATP J. Mol. Biol. 334 2003 949 965 (Pubitemid 37485682)
12. E. Antony, and M.M. Hingorani Mismatch recognition-coupled stabilization of Msh2-Msh6 in an ATP-bound state at the initiation of DNA repair Biochemistry 42 2003 7682 7693 (Pubitemid 36758933)
13. E. Antony, and M.M. Hingorani Asymmetric ATP binding and hydrolysis activity of the Thermus aquaticus MutS dimer is key to modulation of its interactions with mismatched DNA Biochemistry 43 2004 13115 13128 (Pubitemid 39362780)
14. S. Gradia, and D. Subramanian R. Fishel hMSH2-hMSH6 forms a hydrolysis-independent sliding clamp on mismatched DNA Mol. Cell 3 1999 255 261 (Pubitemid 29292626)
15. D. Martik, C. Baitinger, and P. Modrich Differential specificities and simultaneous occupancy of human MutSα nucleotide binding sites J. Biol. Chem. 279 2004 28402 28410 (Pubitemid 38900120)
16. B. Studamire, T. Quach, and E. Alani Saccharomyces cerevisiae Msh2p and Msh6p ATPase activities are both required during mismatch repair Mol. Cell. Biol. 18 1998 7590 7601 (Pubitemid 28533078)
17. D.J. Mazur, M.L. Mendillo, and R.D. Kolodner Inhibition of Msh6 ATPase activity by mispaired DNA induces a Msh2(ATP)-Msh6(ATP) state capable of hydrolysis-independent movement along DNA Mol. Cell 22 2006 39 49
18. M.H. Lamers, and D. Georgijevic T.K. Sixma ATP increases the affinity between MutS ATPase domains. Implications for ATP hydrolysis and conformational changes J. Biol. Chem. 279 2004 43879 43885 (Pubitemid 39390695)
19. E. Alani, and J.Y. Lee W. Yang Crystal structure and biochemical analysis of the MutS.ADP.beryllium fluoride complex suggests a conserved mechanism for ATP interactions in mismatch repair J. Biol. Chem. 278 2003 16088 16094 (Pubitemid 36799730)
20. G. Obmolova, and C. Ban W. Yang Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA Nature 407 2000 703 710
21. M.H. Lamers, H.H. Winterwerp, and T.K. Sixma The alternating ATPase domains of MutS control DNA mismatch repair EMBO J. 22 2003 746 756 (Pubitemid 36193618)
22. G. Natrajan, and M.H. Lamers T.K. Sixma Structures of Escherichia coli DNA mismatch repair enzyme MutS in complex with different mismatches: a common recognition mode for diverse substrates Nucleic Acids Res. 31 2003 4814 4821 (Pubitemid 37441845)
23. J.J. Warren, and T.J. Pohlhaus L.S. Beese Structure of the human MutSalpha DNA lesion recognition complex Mol. Cell 26 2007 579 592 (Pubitemid 46765184)
24. M.S. Junop, and G. Obmolova W. Yang Composite active site of an ABC ATPase: MutS uses ATP to verify mismatch recognition and authorize DNA repair Mol. Cell 7 2001 1 12 (Pubitemid 32162894)
25. M.L. Mendillo, and C.D. Putnam R.D. Kolodner Probing DNA- and ATP-mediated conformational changes in the MutS family of mispair recognition proteins using deuterium exchange mass spectrometry J. Biol. Chem. 285 2010 13170 13182
26. S. Mukherjee, and M. Feig Conformational change in MSH2-MSH6 upon binding DNA coupled to ATPase activity Biophys. J. 96 2009 L63 L65
27. S. Mukherjee, S.M. Law, and M. Feig Deciphering the mismatch recognition cycle in MutS and MSH2-MSH6 using normal-mode analysis Biophys. J. 96 2009 1707 1720
28. V.A. Malkov, and I. Biswas P. Hsieh Photocross-linking of the NH2-terminal region of Taq MutS protein to the major groove of a heteroduplex DNA J. Biol. Chem. 272 1997 23811 23817 (Pubitemid 27410960)
29. P. Dufner, and G. Marra J. Jiricny Mismatch recognition and DNA-dependent stimulation of the ATPase activity of hMutSα is abolished by a single mutation in the hMSH6 subunit J. Biol. Chem. 275 2000 36550 36555 (Pubitemid 32002052)
30. J. Zhai, and M.M. Hingorani Saccharomyces cerevisiae Msh2-Msh6 DNA binding kinetics reveal a mechanism of targeting sites for DNA mismatch repair Proc. Natl. Acad. Sci. USA 107 2010 680 685
31. D.E.J. Koshland Jr., G. Némethy, and D. Filmer Comparison of experimental binding data and theoretical models in proteins containing subunits Biochemistry 5 1966 365 385
32. J. Monod, J. Wyman, and J.P. Changeux On the nature of allosteric transitions: a plausible model J. Mol. Biol. 12 1965 88 118
33. D.A. Case, and T.A. Darden P.A. Kollman AMBER 9 2006 University of California San Francisco
34. W.D. Cornell, and P. Cieplak P.A. Kollman A second generation force field for the simulation of proteins, nucleic acids, and organic molecules J. Am. Chem. Soc. 117 1995 5179 5197
35. J. Wang, P. Cieplak, and P.A. Kollman How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 21 2000 1049 1074
36. V. Hornak, and R. Abel C. Simmerling Comparison of multiple Amber force fields and development of improved protein backbone parameters Proteins 65 2006 712 725 (Pubitemid 44583220)
37. A. Pérez, and I. Marchán M. Orozco Refinement of the AMBER force field for nucleic acids: improving the description of α/γ conformers Biophys. J. 92 2007 3817 3829 (Pubitemid 46910569)
38. I.S. Joung, and T.E. Cheatham 3rd Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations J. Phys. Chem. B 112 2008 9020 9041
39. K.L. Meagher, L.T. Redman, and H.A. Carlson Development of polyphosphate parameters for use with the AMBER force field J. Comput. Chem. 24 2003 1016 1025
40. W.L. Jorgensen, and J. Chandrasekhar M.L. Klein Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79 1983 926 935
41. T.A. Darden, D. York, and L. Pedersen Particle mesh Ewald - an Nlog(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
42. U. Essmann, and L. Perera L.G. Pedersen A smooth particle mesh Ewald method J. Chem. Phys. 103 1995 8577 8593
43. M.F. Crowley, and T.A. Darden D.W. Deerfield II Adventures in improving the scaling and accuracy of a parallel molecular dynamics program J. Supercomput. 11 1997 255 278 (Pubitemid 127507287)
44. H.J.C. Berendsen, and J.P.M. Postma J.R. Haak Molecular dynamics with coupling to an external heath bath J. Chem. Phys. 81 1984 3684 3690
45. J.-P. Ryckaert, G. Ciccotti, and H.J. Berendsen Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes J. Comput. Phys. 23 1977 327 341
46. A. Grossfield, and D.M. Zuckerman Quantifying uncertainty and sampling quality in biomolecular simulations Annu Rep Comput Chem. 5 2009 23 48
47. R.M. Levy, and A.R. Srinivasan J.A. McCammon Quasi-harmonic method for studying very low frequency modes in proteins Biopolymers 23 1984 1099 1112
48. A. Amadei, A.B. Linssen, and H.J. Berendsen Essential dynamics of proteins Proteins 17 1993 412 425 (Pubitemid 23358549)
49. T. Ichiye, and M. Karplus Collective motions in proteins: a covariance analysis of atomic fluctuations in molecular dynamics and normal mode simulations Proteins 11 1991 205 217
50. Cheatham III, T. E. 2008. Ptraj, AmberTools 1.2.
51. I. Biswas, and R. Vijayvargia Heteroduplex DNA and ATP induced conformational changes of a MutS mismatch repair protein from Thermus aquaticus Biochem. J. 347 2000 881 886 (Pubitemid 30260981)
52. C. Jeong, and W.K. Cho J.B. Lee MutS switches between two fundamentally distinct clamps during mismatch repair Nat. Struct. Mol. Biol. 18 2011 379 385
53. C.J. Tsai, A. del Sol, and R. Nussinov Allostery: absence of a change in shape does not imply that allostery is not at play J. Mol. Biol. 378 2008 1 11
54. K. Gunasekaran, B.Y. Ma, and R. Nussinov Is allostery an intrinsic property of all dynamic proteins? Proteins 57 2004 433 443 (Pubitemid 39390799)
55. A. Cooper, and D.T. Dryden Allostery without conformational change. A plausible model Eur. Biophys. J. 11 1984 103 109
56. M. Karplus, and T. Ichiye Comment on a "fluctuation and cross correlation analysis of protein motions observed in nanosecond molecular dynamics simulations" J. Mol. Biol. 263 1996 120 122 (Pubitemid 26363075)
57. W.E. Harte Jr., and S. Swaminathan D.L. Beveridge Domain communication in the dynamical structure of human immunodeficiency virus 1 protease Proc. Natl. Acad. Sci. USA 87 1990 8864 8868 (Pubitemid 120007609)
58. S. Swaminathan, W.E. Harte Jr., and D.L. Beveridge Investigation of domain structure in proteins via molecular dynamics simulation: application to HIV-1 protease dimer J. Am. Chem. Soc. 113 1991 2717 2721
59. B.L. Kormos, A.M. Baranger, and D.L. Beveridge Do collective atomic fluctuations account for cooperative effects? Molecular dynamics studies of the U1A-RNA complex J. Am. Chem. Soc. 128 2006 8992 8993 (Pubitemid 44078957)
60. B.L. Kormos, A.M. Baranger, and D.L. Beveridge A study of collective atomic fluctuations and cooperativity in the U1A-RNA complex based on molecular dynamics simulations J. Struct. Biol. 157 2007 500 513
61. M.H. Knaggs, and F.R. Salsbury Jr. J.S. Fetrow Insights into correlated motions and long-range interactions in CheY derived from molecular dynamics simulations Biophys. J. 92 2007 2062 2079 (Pubitemid 46495269)
62. R. Abseher, and M. Nilges Are there non-trivial dynamic cross-correlations in proteins? J. Mol. Biol. 279 1998 911 920 (Pubitemid 28284705)
63. P.H. Hünenberger, A.E. Mark, and W.F. van Gunsteren Fluctuation and cross-correlation analysis of protein motions observed in nanosecond molecular dynamics simulations J. Mol. Biol. 252 1995 492 503
64. I. Winkler, and A.D. Marx P. Friedhoff Chemical trapping of the dynamic MutS-MutL complex formed in DNA mismatch repair in Escherichia coli J. Biol. Chem. 286 2011 17326 17337
65. R.G. Smock, and L.M. Gierasch Sending signals dynamically Science 324 2009 198 203
66. N. Popovych, and S.J. Sun C.G. Kalodimos Dynamically driven protein allostery Nat. Struct. Mol. Biol. 13 2006 831 838 (Pubitemid 44338778)
67. J.P. Changeux, and S.J. Edelstein Allosteric mechanisms of signal transduction Science 308 2005 1424 1428 (Pubitemid 40791288)
68. T. Schirmer, and P.R. Evans Structural basis of the allosteric behaviour of phosphofructokinase Nature 343 1990 140 145
69. F.R. Salsbury Jr., and J.E. Clodfelter K.D. Scarpinato The molecular mechanism of DNA damage recognition by MutS homologs and its consequences for cell death response Nucleic Acids Res. 34 2006 2173 2185 (Pubitemid 43985656)
70. J. Gorman, and A. Chowdhury E.C. Greene Dynamic basis for one-dimensional DNA scanning by the mismatch repair complex Msh2-Msh6 Mol. Cell 28 2007 359 370 (Pubitemid 350030566)